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Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Systematic Review Article

Citrus Flavonoids and Autoimmune Diseases: A Systematic Review of Clinical Studies

Author(s): Laura Musumeci, Alessandro Maugeri, Caterina Russo, Giovanni Enrico Lombardo*, Santa Cirmi* and Michele Navarra

Volume 30, Issue 19, 2023

Published on: 03 October, 2022

Page: [2191 - 2204] Pages: 14

DOI: 10.2174/0929867329666220629144744

Price: $65

Abstract

Background: Autoimmune diseases are chronic disorders in which the immune system does not recognize and attacks one self’s healthy components. In this context, although natural remedies might represent a promising therapeutic strategy, evidence regarding Citrus flavonoids is still controversial.

Objective: To summarize and critically discuss the clinical evidence on the effects of Citrus flavonoids on managing autoimmune diseases.

Method: A systematic review of articles has been carried out independently by two authors using MEDLINE, Scopus and ISI Web of Science databases. Search terms comprised keywords related to Citrus flavonoids and autoimmune diseases. The last search was performed on the 16th of March, 2021. No language restrictions were applied. Systematic review and study selection were conducted in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement. Before starting the review, the authors defined the types of articles to be included. Three reviewers independently carried out the extraction of papers.

Results: Ten clinical studies fulfilled the eligibility criteria and were included in the final review.

Conclusion: The studies discussed in this review are heterogeneous. Indeed, some studies suggest using Citrus flavonoids in the frame of autoimmune disorders, whereas others discourage it. Hence, this systematic review highlights the need for further large-scale clinical studies to define the exact role of Citrus flavonoids in managing autoimmune diseases (PROSPERO number CRD42021234903).

Keywords: autoimmune diseases, immune system, Citrus flavonoids, natural compounds, nutraceuticals; clinical studies, systematic review, supplement, rheumatoid arthritis, psoriasis, diabetes, colitis, thyroiditis

[1]
Rosenblum, M.D.; Remedios, K.A.; Abbas, A.K. Mechanisms of human autoimmunity. J. Clin. Invest., 2015, 125(6), 2228-2233.
[http://dx.doi.org/10.1172/JCI78088] [PMID: 25893595]
[2]
Migliorini, P.; Italiani, P.; Pratesi, F.; Puxeddu, I.; Boraschi, D. The IL-1 family cytokines and receptors in autoimmune diseases. Autoimmun. Rev., 2020, 19(9), 102617.
[http://dx.doi.org/10.1016/j.autrev.2020.102617] [PMID: 32663626]
[3]
Di Salvo, E.; Ventura-Spagnolo, E.; Casciaro, M.; Navarra, M.; Gangemi, S. IL-33/IL-31 Axis: A potential inflammatory pathway. Mediators Inflamm., 2018, 2018, 1-8.
[http://dx.doi.org/10.1155/2018/3858032] [PMID: 29713240]
[4]
Simoni, Y.; Diana, J.; Ghazarian, L.; Beaudoin, L.; Lehuen, A. Therapeutic manipulation of natural killer (NK) T cells in autoimmunity: Are we close to reality? Clin. Exp. Immunol., 2012, 171(1), 8-19.
[http://dx.doi.org/10.1111/j.1365-2249.2012.04625.x] [PMID: 23199318]
[5]
Morandi, B.; Bramanti, P.; Bonaccorsi, I.; Montalto, E.; Oliveri, D.; Pezzino, G.; Navarra, M.; Ferlazzo, G. Role of natural killer cells in the pathogenesis and progression of multiple sclerosis. Pharmacol. Res., 2008, 57(1), 1-5.
[http://dx.doi.org/10.1016/j.phrs.2007.11.003] [PMID: 18182304]
[6]
Autoimmune Association. Autoimmune Diseases List, 2021. Available from: https://www.aarda.org/diseaselist/
[7]
Alexander, T.; Bondanza, A.; Muraro, P.A.; Greco, R.; Saccardi, R.; Daikeler, T.; Kazmi, M.; Hawkey, C.; Simoes, B.P.; Leblanc, K.; Fibbe, W.E.; Moore, J.; Snarski, E.; Martin, T.; Hiepe, F.; Velardi, A.; Toubert, A.; Snowden, J.A.; Farge, D. SCT for severe autoimmune diseases: Consensus guidelines of the european society for blood and marrow transplantation for immune monitoring and biobanking. Bone Marrow Transplant., 2015, 50(2), 173-180.
[http://dx.doi.org/10.1038/bmt.2014.251] [PMID: 25387090]
[8]
Lerner, A.; Jeremias, P.; Matthias, T. The world incidence and prevalence of autoimmune diseases is increasing. Int. Int. Celiac Dis., 2016, 3(4), 151-155.
[http://dx.doi.org/10.12691/ijcd-3-4-8]
[9]
Mastrandrea, L.D. An overview of organ-specific autoimmune diseases including immunotherapy. Immunol. Invest., 2015, 44(8), 803-816.
[http://dx.doi.org/10.3109/08820139.2015.1099409] [PMID: 26575465]
[10]
Wahren-Herlenius, M.; Dörner, T. Immunopathogenic mechanisms of systemic autoimmune disease. Lancet, 2013, 382(9894), 819-831.
[http://dx.doi.org/10.1016/S0140-6736(13)60954-X] [PMID: 23993191]
[11]
Banchereau, R.; Cepika, A.M.; Pascual, V. Systems approaches to human autoimmune diseases. Curr. Opin. Immunol., 2013, 25(5), 598-605.
[http://dx.doi.org/10.1016/j.coi.2013.08.005] [PMID: 24055331]
[12]
Duan, L.; Rao, X.; Sigdel, K.R. Regulation of inflammation in autoimmune disease. J. Immunol. Res., 2019, 2019, 1-2.
[http://dx.doi.org/10.1155/2019/7403796] [PMID: 30944837]
[13]
Wójcik, P.; Gęgotek, A.; Žarković, N.; Skrzydlewska, E. Oxidative stress and lipid mediators modulate immune cell functions in autoimmune diseases. Int. J. Mol. Sci., 2021, 22(2), 723.
[http://dx.doi.org/10.3390/ijms22020723] [PMID: 33450863]
[14]
Konforte, D.; Diamandis, E.P.; van Venrooij, W.J.; Lories, R.; Ward, M.M. Autoimmune diseases: Early diagnosis and new treatment strategies. Clin. Chem., 2012, 58(11), 1510-1514.
[http://dx.doi.org/10.1373/clinchem.2012.189480] [PMID: 22761474]
[15]
Rengasamy, K.R.R.; Khan, H.; Gowrishankar, S.; Lagoa, R.J.L.; Mahomoodally, F.M.; Khan, Z.; Suroowan, S.; Tewari, D.; Zengin, G.; Hassan, S.T.S.; Pandian, S.K. The role of flavonoids in autoimmune diseases: Therapeutic updates. Pharmacol. Ther., 2019, 194, 107-131.
[http://dx.doi.org/10.1016/j.pharmthera.2018.09.009] [PMID: 30268770]
[16]
Lee, J.I.; Park, K.S.; Cho, I.H. Panax ginseng: A candidate herbal medicine for autoimmune disease. J. Ginseng Res., 2019, 43(3), 342-348.
[http://dx.doi.org/10.1016/j.jgr.2018.10.002] [PMID: 31308804]
[17]
Venkatesha, S.H.; Astry, B.; Nanjundaiah, S.M.; Kim, H.R.; Rajaiah, R.; Yang, Y.; Tong, L.; Yu, H.; Berman, B.M.; Moudgil, K.D. Control of autoimmune arthritis by herbal extracts and their bioactive components. Asian J. Pharmaceut. Sci., 2016, 11(2), 301-307.
[18]
Zampieron, E.R.; Kamhi, E.J. Natural support for autoimmune and inflammatory disease. J. Restor. Med., 2012, 1(1), 38-47.
[http://dx.doi.org/10.14200/jrm.2012.1.1003]
[19]
Daily, J.W.; Yang, M.; Park, S. Efficacy of turmeric extracts and curcumin for alleviating the symptoms of joint arthritis: A systematic review and meta-analysis of randomized clinical trials. J. Med. Food, 2016, 19(8), 717-729.
[http://dx.doi.org/10.1089/jmf.2016.3705] [PMID: 27533649]
[20]
Khan, M.K.; Zill-E-Huma; Dangles, O. A comprehensive review on flavanones, the major citrus polyphenols. J. Food Compos. Anal., 2014, 33(1), 85-104.
[http://dx.doi.org/10.1016/j.jfca.2013.11.004]
[21]
Felice, M.R.; Maugeri, A.; De Sarro, G.; Navarra, M.; Barreca, D. Molecular pathways involved in the anti-cancer activity of flavonols: A focus on myricetin and kaempferol. IJMS, 2022. [Epub ahead of print].
[22]
Cirmi, S.; Maugeri, A.; Ferlazzo, N.; Gangemi, S.; Calapai, G.; Schumacher, U.; Navarra, M. Anticancer potential of citrus juices and their extracts: A systematic review of both preclinical and clinical studies. Front. Pharmacol., 2017, 8, 420.
[http://dx.doi.org/10.3389/fphar.2017.00420] [PMID: 28713272]
[23]
Cirmi, S.; Bisignano, C.; Mandalari, G.; Navarra, M. Anti-infective potential of Citrus bergamia risso et poiteau (bergamot) derivatives: A systematic review. Phytother. Res., 2016, 30(9), 1404-1411.
[http://dx.doi.org/10.1002/ptr.5646] [PMID: 27218799]
[24]
Cirmi, S.; Ferlazzo, N.; Lombardo, G.; Ventura-Spagnolo, E.; Gangemi, S.; Calapai, G.; Navarra, M. Neurodegenerative diseases: Might citrus flavonoids play a protective role? Molecules, 2016, 21(10), 1312.
[http://dx.doi.org/10.3390/molecules21101312] [PMID: 27706034]
[25]
Russo, C.; Maugeri, A.; Lombardo, G.E.; Musumeci, L.; Barreca, D.; Rapisarda, A.; Cirmi, S.; Navarra, M. The second life of citrus fruit waste: A valuable source of bioactive compounds. Molecules, 2021, 26(19), 5991.
[http://dx.doi.org/10.3390/molecules26195991] [PMID: 34641535]
[26]
Mannucci, C.; Navarra, M.; Calapai, F.; Squeri, R.; Gangemi, S.; Calapai, G. Clinical pharmacology of Citrus bergamia : A systematic review. Phytother. Res., 2017, 31(1), 27-39.
[http://dx.doi.org/10.1002/ptr.5734] [PMID: 27747942]
[27]
Mannucci, C.; Calapai, F.; Cardia, L.; Inferrera, G.; D'Arena, G.; Di Pietro, M.; Navarra, M.; Gangemi, S.; Ventura Spagnolo, E.; Calapai, G. Clinical pharmacology of citrus aurantium and citrus sinensis for the treatment of anxiety. Evid.-Based Complement. Altern. Med., 2018, 2018, 3624094.
[28]
Abad-García, B.; Garmón-Lobato, S.; Sánchez-Ilárduya, M.B.; Berrueta, L.A.; Gallo, B.; Vicente, F.; Alonso-Salces, R.M. Polyphenolic contents in citrus fruit juices: Authenticity assessment. Eur. Food Res. Technol., 2014, 238(5), 803-818.
[http://dx.doi.org/10.1007/s00217-014-2160-9]
[29]
Wang, S.; Yang, C.; Tu, H.; Zhou, J.; Liu, X.; Cheng, Y.; Luo, J.; Deng, X.; Zhang, H.; Xu, J. Characterization and metabolic diversity of flavonoids in citrus species. Sci. Rep., 2017, 7(1), 10549.
[http://dx.doi.org/10.1038/s41598-017-10970-2] [PMID: 28874745]
[30]
Wen, K.; Fang, X.; Yang, J.; Yao, Y.; Nandakumar, K.S.; Salem, M.L.; Cheng, K. Recent research on flavonoids and their biomedical applications. Curr. Med. Chem., 2021, 28(5), 1042-1066.
[http://dx.doi.org/10.2174/0929867327666200713184138] [PMID: 32660393]
[31]
Filocamo, A.; Bisignano, C.; Ferlazzo, N.; Cirmi, S.; Mandalari, G.; Navarra, M. in vitro effect of bergamot (Citrus bergamia) juice against caga-positive and-negative clinical isolates of helicobacter pylori. BMC Complement. Altern. Med., 2015, 15(1), 256.
[http://dx.doi.org/10.1186/s12906-015-0769-2] [PMID: 26220068]
[32]
Hernández, A.; Ruiz-Moyano, S.; Galván, A.I.; Merchán, A.V.; Pérez Nevado, F.; Aranda, E.; Serradilla, M.J.; Córdoba, M.G.; Martín, A. Anti-fungal activity of phenolic sweet orange peel extract for controlling fungi responsible for post-harvest fruit decay. Fungal Biol., 2021, 125(2), 143-152.
[http://dx.doi.org/10.1016/j.funbio.2020.05.005] [PMID: 33518204]
[33]
Navarra, M.; Femia, A.P.; Romagnoli, A.; Tortora, K.; Luceri, C.; Cirmi, S.; Ferlazzo, N.; Caderni, G. A flavonoid-rich extract from bergamot juice prevents carcinogenesis in a genetic model of colorectal cancer, the Pirc rat (F344/NTac-Apcam1137). Eur. J. Nutr., 2020, 59(3), 885-894.
[http://dx.doi.org/10.1007/s00394-019-01948-z] [PMID: 30919084]
[34]
Celano, M.; Maggisano, V.; De Rose, R.F.; Bulotta, S.; Maiuolo, J.; Navarra, M.; Russo, D. Flavonoid fraction of Citrus reticulata juice reduces proliferation and migration of anaplastic thyroid carcinoma cells. Nutr. Cancer, 2015, 67(7), 1183-1190.
[http://dx.doi.org/10.1080/01635581.2015.1073760] [PMID: 26365817]
[35]
Maugeri, A.; Lombardo, G.E.; Musumeci, L.; Russo, C.; Gangemi, S.; Calapai, G.; Cirmi, S.; Navarra, M. Bergamottin and 5-geranyloxy-7-methoxycoumarin cooperate in the cytotoxic effect of Citrus bergamia (bergamot) essential oil in human neuroblastoma sh-sy5y cell line. Toxins (Basel), 2021, 13(4), 275.
[http://dx.doi.org/10.3390/toxins13040275] [PMID: 33920139]
[36]
Citraro, R.; Navarra, M.; Leo, A.; Donato Di Paola, E.; Santangelo, E.; Lippiello, P.; Aiello, R.; Russo, E.; De Sarro, G. The anticonvulsant activity of a flavonoid-rich extract from orange juice involves both nmda and gaba-benzodiazepine receptor complexes. Molecules, 2016, 21(9), 1261.
[http://dx.doi.org/10.3390/molecules21091261] [PMID: 27657037]
[37]
Cirmi, S.; Maugeri, A.; Lombardo, G.E.; Russo, C.; Musumeci, L.; Gangemi, S.; Calapai, G.; Barreca, D.; Navarra, M. A flavonoid-rich extract of mandarin juice counteracts 6-ohda-induced oxidative stress in sh-sy5y cells and modulates parkinson-related genes. Antioxidants, 2021, 10(4), 539.
[http://dx.doi.org/10.3390/antiox10040539] [PMID: 33808343]
[38]
Ferlazzo, N.; Cirmi, S.; Maugeri, A.; Russo, C.; Lombardo, G.E.; Gangemi, S.; Calapai, G.; Mollace, V.; Navarra, M. Neuroprotective effect of bergamot juice in 6-ohda-induced sh-sy5y cell death, an in vitro model of parkinson’s disease. Pharmaceutics, 2020, 12(4), 326.
[http://dx.doi.org/10.3390/pharmaceutics12040326] [PMID: 32260543]
[39]
Montalbano, G.; Mania, M.; Guerrera, M.C.; Laurà, R.; Abbate, F.; Levanti, M.; Maugeri, A.; Germanà, A.; Navarra, M. Effects of a flavonoid-rich extract from Citrus sinensis juice on a diet-induced obese zebrafish. Int. J. Mol. Sci., 2019, 20(20), 5116.
[http://dx.doi.org/10.3390/ijms20205116] [PMID: 31619003]
[40]
Park, J.; Kim, H.L.; Jung, Y.; Ahn, K.S.; Kwak, H.J.; Um, J.Y. Bitter orange (citrus aurantium linné) improves obesity by regulating adipogenesis and thermogenesis through ampk activation. Nutrients, 2019, 11(9), 1988.
[http://dx.doi.org/10.3390/nu11091988] [PMID: 31443565]
[41]
Maugeri, A.; Ferlazzo, N.; De Luca, L.; Gitto, R.; Navarra, M. The link between the AMPK/SIRT1 axis and a flavonoid-rich extract of Citrus bergamia juice: A cell-free, in silico, and in vitro study. Phytother. Res., 2019, 33(7), 1805-1814.
[http://dx.doi.org/10.1002/ptr.6368] [PMID: 31094018]
[42]
Currò, M.; Risitano, R.; Ferlazzo, N.; Cirmi, S.; Gangemi, C.; Caccamo, D.; Ientile, R.; Navarra, M. Citrus bergamia juice extract attenuates β-amyloid-induced pro-inflammatory activation of thp-1 cells through mapk and ap-1 pathways. Sci. Rep., 2016, 6(1), 20809.
[http://dx.doi.org/10.1038/srep20809] [PMID: 26853104]
[43]
Lombardo, G.E.; Cirmi, S.; Musumeci, L.; Pergolizzi, S.; Maugeri, A.; Russo, C.; Mannucci, C.; Calapai, G.; Navarra, M. Mechanisms underlying the anti-inflammatory activity of bergamot essential oil and its antinociceptive effects. Plants, 2020, 9(6), 704.
[http://dx.doi.org/10.3390/plants9060704] [PMID: 32492797]
[44]
Cirmi, S.; Randazzo, B.; Russo, C.; Musumeci, L.; Maugeri, A.; Montalbano, G.; Guerrera, M.C.; Lombardo, G.E.; Levanti, M. Anti-inflammatory effect of a flavonoid-rich extract of orange juice in adult zebrafish subjected to Vibrio anguillarum-induced enteritis. Nat. Prod. Res., 2020, 35(23), 5350-5353.
[PMID: 32338069]
[45]
Gugliandolo, E.; Fusco, R.; D’Amico, R.; Peditto, M.; Oteri, G.; Di Paola, R.; Cuzzocrea, S.; Navarra, M. Treatment with a flavonoid-rich fraction of bergamot juice improved lipopolysaccharide-induced periodontitis in rats. Front. Pharmacol., 2019, 9, 1563.
[http://dx.doi.org/10.3389/fphar.2018.01563] [PMID: 30705631]
[46]
Fusco, R.; Cirmi, S.; Gugliandolo, E.; Di Paola, R.; Cuzzocrea, S.; Navarra, M. A flavonoid-rich extract of orange juice reduced oxidative stress in an experimental model of inflammatory bowel disease. J. Funct. Foods, 2017, 30, 168-178.
[http://dx.doi.org/10.1016/j.jff.2016.12.038]
[47]
Ferlazzo, N.; Micali, A.; Marini, H.R.; Freni, J.; Santoro, G.; Puzzolo, D.; Squadrito, F.; Pallio, G.; Navarra, M.; Cirmi, S.; Minutoli, L. A flavonoid-rich extract from bergamot juice, alone or in association with curcumin and resveratrol, shows protective effects in a murine model of cadmium-induced testicular injury. Pharmaceuticals (Basel), 2021, 14(5), 386.
[http://dx.doi.org/10.3390/ph14050386] [PMID: 33919028]
[48]
Mannucci, C.; Casciaro, M.; Sorbara, E.E.; Calapai, F.; Di Salvo, E.; Pioggia, G.; Navarra, M.; Calapai, G.; Gangemi, S. Nutraceuticals against oxidative stress in autoimmune disorders. Antioxidants, 2021, 10(2), 261.
[http://dx.doi.org/10.3390/antiox10020261] [PMID: 33567628]
[49]
Ferlazzo, N.; Visalli, G.; Cirmi, S.; Lombardo, G.E.; Laganà, P.; Di Pietro, A.; Navarra, M. Natural iron chelators: Protective role in a549 cells of flavonoids-rich extracts of citrus juices in fe 3+ -induced oxidative stress. Environ. Toxicol. Pharmacol., 2016, 43, 248-256.
[http://dx.doi.org/10.1016/j.etap.2016.03.005] [PMID: 27037654]
[50]
Ferlazzo, N.; Visalli, G.; Smeriglio, A.; Cirmi, S.; Lombardo, G.E.; Campiglia, P.; Di Pietro, A.; Navarra, M. Flavonoid fraction of orange and bergamot juices protect human lung epithelial cells from hydrogen peroxide-induced oxidative stress. Evid.-Based Complement. Altern. Med., 2015, 2015, 957031.
[51]
Haddad, P.; Eid, H. The antidiabetic potential of quercetin: Underlying mechanisms. Curr. Med. Chem., 2017, 24(4), 355-364.
[http://dx.doi.org/10.2174/0929867323666160909153707] [PMID: 27633685]
[52]
Musumeci, L.; Maugeri, A.; Cirmi, S.; Lombardo, G.E.; Russo, C.; Gangemi, S.; Calapai, G.; Navarra, M. Citrus fruits and their flavonoids in inflammatory bowel disease: An overview. Nat. Prod. Res., 2020, 34(1), 122-136.
[http://dx.doi.org/10.1080/14786419.2019.1601196] [PMID: 30990326]
[53]
Maugeri, A.; Cirmi, S.; Minciullo, P.L.; Gangemi, S.; Calapai, G.; Mollace, V.; Navarra, M. Citrus fruits and inflammaging: A systematic review. Phytochem. Rev., 2019, 18(4), 1025-1049.
[http://dx.doi.org/10.1007/s11101-019-09613-3]
[54]
Verbeek, R.; van Tol, E.A.F.; van Noort, J.M. Oral flavonoids delay recovery from experimental autoimmune encephalomyelitis in SJL mice. Biochem. Pharmacol., 2005, 70(2), 220-228.
[http://dx.doi.org/10.1016/j.bcp.2005.04.041] [PMID: 15946653]
[55]
Autoimmune Registry. Donate to the immune registery. 2021. Available from: https://www.autoimmuneregistry.org/autoimmune-diseases
[56]
Page, M.J.; McKenzie, J.E.; Bossuyt, P.M.; Boutron, I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; Akl, E.A.; Brennan, S.E.; Chou, R.; Glanville, J.; Grimshaw, J.M.; Hróbjartsson, A.; Lalu, M.M.; Li, T.; Loder, E.W.; Mayo-Wilson, E.; McDonald, S.; McGuinness, L.A.; Stewart, L.A.; Thomas, J.; Tricco, A.C.; Welch, V.A.; Whiting, P.; Moher, D. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. BMJ, 2021, 372(71), n71.
[http://dx.doi.org/10.1136/bmj.n71] [PMID: 33782057]
[57]
Brembach, H. [Therapy of psoriasis and other skin diseases with rutin and calcium]. Munch. Med. Wochenschr., 1952, 94(29), 1475-1478.
[PMID: 12982838]
[58]
Dzutseva, E.I.; Kulagin, V.I.; Burova, S.A.; Davydova, T.V.; Zubrikhina, G.N.; Gorozhanskaia, E.G. Effect of diquertin on the intensity of lipid peroxidation in patients with diabetes mellitus in the treatment of nail mycosis. Klin. Lab. Diagn., 2003, (4), 11-13.
[PMID: 12774661]
[59]
Manuel y Keenoy, B.; Vertommen, J.; De Leeuw, I. The effect of flavonoid treatment on the glycation and antioxidant status in Type 1 diabetic patients. Diabetes Nutr. Metab., 1999, 12(4), 256-263.
[PMID: 10782751]
[60]
Polushina, N.D.; Kartazaeva, V.A.; Botvineva, L.A.; Kozhevnikov, S.A. The effects of the combined use of mineral water with ascorbic acid and rutin experimentally and clinically. Vopr. Kurortol. Fizioter. Lech. Fiz. Kult., 2000, (2), 31-34.
[PMID: 11094893]
[61]
Schnellen, B. New possibilities in the therapy of psoriasis. Z. Hautkr., 1977, 52(8), 466-469.
[PMID: 868200]
[62]
Shevchuk, S.V.; Stanislavchuk, M.A.; Pentiuk, O.O. Efficacy and safety of treatment with methotrexate, leflunomide, detralex, and their combination of patients with rheumatoid arthritis. Lik. Sprava, 2003, (3-4), 34-41.
[PMID: 12889354]
[63]
Warter, P.J.; Drezner, H.L.; Horoschak, S. Effect of hesperidin and ascorbic acid on capillary fragility in rheumatoid arthritis; a preliminary report. J. Med. Soc. N. J., 1946, 43, 228-230.
[PMID: 20986079]
[64]
Warter, P.J.; Drezner, H.L.; Horoschak, S. The influence of hesperidin-C on abnormal capillary fragility in rheumatoid arthritis patients. Del. Med. J., 1948, 20(3), 41-45.
[PMID: 18862295]
[65]
Bae, S.C.; Jung, W.J.; Lee, E.J.; Yu, R.; Sung, M.K. Effects of antioxidant supplements intervention on the level of plasma inflammatory molecules and disease severity of rheumatoid arthritis patients. J. Am. Coll. Nutr., 2009, 28(1), 56-62.
[http://dx.doi.org/10.1080/07315724.2009.10719762] [PMID: 19571161]
[66]
Hickson, L.J.; Langhi Prata, L.G.P.; Bobart, S.A.; Evans, T.K.; Giorgadze, N.; Hashmi, S.K.; Herrmann, S.M.; Jensen, M.D.; Jia, Q.; Jordan, K.L.; Kellogg, T.A.; Khosla, S.; Koerber, D.M.; Lagnado, A.B.; Lawson, D.K.; LeBrasseur, N.K.; Lerman, L.O.; McDonald, K.M.; McKenzie, T.J.; Passos, J.F.; Pignolo, R.J.; Pirtskhalava, T.; Saadiq, I.M.; Schaefer, K.K.; Textor, S.C.; Victorelli, S.G.; Volkman, T.L.; Xue, A.; Wentworth, M.A.; Wissler Gerdes, E.O.; Zhu, Y.; Tchkonia, T.; Kirkland, J.L. Senolytics decrease senescent cells in humans: Preliminary report from a clinical trial of dasatinib plus quercetin in individuals with diabetic kidney disease. EBioMedicine, 2019, 47, 446-456.
[http://dx.doi.org/10.1016/j.ebiom.2019.08.069] [PMID: 31542391]
[67]
Harada, N.; Okajima, K. Effects of capsaicin and isoflavone on blood pressure and serum levels of insulin-like growth factor-I in normotensive and hypertensive volunteers with alopecia. Biosci. Biotechnol. Biochem., 2009, 73(6), 1456-1459.
[http://dx.doi.org/10.1271/bbb.80883] [PMID: 19502719]
[68]
Harada, N.; Okajima, K.; Arai, M.; Kurihara, H.; Nakagata, N. Administration of capsaicin and isoflavone promotes hair growth by increasing insulin-like growth factor-I production in mice and in humans with alopecia. Growth Hormone IGF Res., 2007, 17(5), 408-415.
[69]
Kempf, K.; Manzo, G.; Hanifi-Moghaddam, P.; Kappler, S.; Seissler, J.; Jaeger, C.; Boehm, B.; Roden, M.; Kolb, H.; Martin, S.; Schloot, N.C. Effect of combined oral proteases and flavonoid treatment in subjects at risk of type 1 diabetes. Diabet. Med., 2009, 26(12), 1309-1310.
[http://dx.doi.org/10.1111/j.1464-5491.2009.02879.x] [PMID: 20002490]
[70]
Matsuno, H.; Nakamura, H.; Katayama, K.; Hayashi, S.; Kano, S.; Yudoh, K.; Kiso, Y. Effects of an oral administration of glucosamine-chondroitin-quercetin glucoside on the synovial fluid properties in patients with osteoarthritis and rheumatoid arthritis. Biosci. Biotechnol. Biochem., 2009, 73(2), 288-292.
[http://dx.doi.org/10.1271/bbb.80418] [PMID: 19202302]
[71]
Valensi, P.; Le Devehat, C.; Richard, J.L.; Farez, C.; Khodabandehlou, T.; Rosenbloom, R.A.; LeFante, C. A multicenter, double-blind, safety study of QR-333 for the treatment of symptomatic diabetic peripheral neuropathy. J. Diabetes Complicat., 2005, 19(5), 247-253.
[http://dx.doi.org/10.1016/j.jdiacomp.2005.05.011] [PMID: 16112498]
[72]
de Font-Réaulx Rojas, E.; Dorazco-Barragán, G. Clinical stabilisation in neurodegenerative diseases: Clinical study in phase II. Rev. Neurol., 2010, 50(9), 520-528.
[PMID: 20443170]
[73]
Cuervo, A.; Hevia, A.; López, P.; Suárez, A.; Sánchez, B.; Margolles, A.; González, S. Association of polyphenols from oranges and apples with specific intestinal microorganisms in systemic lupus erythematosus patients. Nutrients, 2015, 7(2), 1301-1317.
[http://dx.doi.org/10.3390/nu7021301] [PMID: 25690419]
[74]
Gunns, D.; Leach, M. An increased focus on stress for the management of blood glucose levels in type 1 diabetes: A case report. Australian J. Herbal Naturopathic Med., 2020, 32(1), 10-14.
[http://dx.doi.org/10.33235/32.1.10-14]
[75]
Kometani, T.; Fukuda, T.; Kakuma, T.; Kawaguchi, K.; Tamura, W.; Kumazawa, Y.; Nagata, K. Effects of alpha-glucosylhesperidin, a bioactive food material, on collagen-induced arthritis in mice and rheumatoid arthritis in humans. Immunopharmacol. Immunotoxicol., 2008, 30(1), 117-134.
[http://dx.doi.org/10.1080/08923970701812688] [PMID: 18306109]
[76]
Lu, Y.; Zamora-Ros, R.; Chan, S.; Cross, A.J.; Ward, H.; Jakszyn, P.; Luben, R.; Opstelten, J.L.; Oldenburg, B.; Hallmans, G.; Karling, P.; Grip, O.; Key, T.; Bergmann, M.M.; Boeing, H.; Overvad, K.; Palli, D.; Masala, G.; Khaw, K.T.; Racine, A.; Carbonnel, F.; Boutron-Ruault, M.C.; Andersen, V.; Olsen, A.; Tjonneland, A.; Kaaks, R.; Tumino, R.; Trichopoulou, A.; Scalbert, A.; Riboli, E.; Hart, A.R. Dietary polyphenols in the aetiology of crohnʼs disease and ulcerative colitis—a multicenter european prospective cohort study (EPIC). Inflamm. Bowel Dis., 2017, 23(12), 2072-2082.
[http://dx.doi.org/10.1097/MIB.0000000000001108] [PMID: 28837515]
[77]
Mauriz, E.; Laliena, A.; Vallejo, D.; Tuñón, M.J.; Rodríguez-López, J.M.; Rodríguez-Pérez, R.; García-Fernández, M.C. Effects of a low-fat diet with antioxidant supplementation on biochemical markers of multiple sclerosis long-term care residents. Nutr. Hosp., 2013, 28(6), 2229-2235.
[PMID: 24506405]
[78]
Ardestani, A.; Yazdanparast, R. Flavonoids as potential therapeutic agents for type 1 diabetes. Med. Hypotheses, 2007, 69(4), 955.
[http://dx.doi.org/10.1016/j.mehy.2007.02.001] [PMID: 17433561]
[79]
Bright, J.J. Targeting autoimmune diseases through nutraceuticals. Nutrition, 2004, 20(1), 39-43.
[http://dx.doi.org/10.1016/j.nut.2003.09.007] [PMID: 14698012]
[80]
Magrone, T.; Jirillo, E. The new era of nutraceuticals: Beneficial effects of polyphenols in various experimental and clinical settings. Curr. Pharm. Des., 2019, 24(44), 5229-5231.
[http://dx.doi.org/10.2174/138161282444190329154418] [PMID: 30973101]
[81]
Głąbska, D.; Guzek, D.; Grudzińska, D.; Lech, G. Influence of dietary isoflavone intake on gastrointestinal symptoms in ulcerative colitis individuals in remission. World J. Gastroenterol., 2017, 23(29), 5356-5363.
[http://dx.doi.org/10.3748/wjg.v23.i29.5356] [PMID: 28839435]
[82]
Skolmowska, D.; Głąbska, D.; Guzek, D.; Lech, G. Association between dietary isoflavone intake and ulcerative colitis symptoms in Polish Caucasian individuals. Nutrients, 2019, 11(8), 1936.
[http://dx.doi.org/10.3390/nu11081936] [PMID: 31426486]
[83]
von Hertzen, L.; Forsblom, C.; Stumpf, K.; Pettersson-Fernholm, K.; Adlercreutz, H.; Groop, P.H. Highly elevated serum phyto-oestrogen concentrations in patients with diabetic nephropathy. J. Intern. Med., 2004, 255(5), 602-609.
[http://dx.doi.org/10.1111/j.1365-2796.2004.01330.x] [PMID: 15078503]
[84]
Ohfuji, S.; Fukushima, W.; Watanabe, K.; Sasaki, S.; Yamagami, H.; Nagahori, M.; Watanabe, M.; Hirota, Y. Pre-illness isoflavone consumption and disease risk of ulcerative colitis: A multicenter case-control study in Japan. PLoS One, 2014, 9(10), e110270.
[http://dx.doi.org/10.1371/journal.pone.0110270] [PMID: 25314032]
[85]
Javadi, F.; Eghtesadi, S.; Ahmadzadeh, A.; Aryaeian, N.; Zabihiyeganeh, M.; Foroushani, A.R.; Jazayeri, S. The effect of quercetin on plasma oxidative status, C-reactive protein and blood pressure in women with rheumatoid arthritis. Int. J. Prev. Med., 2014, 5(3), 293-301.
[PMID: 24829713]
[86]
Javadi, F.; Ahmadzadeh, A.; Eghtesadi, S.; Aryaeian, N.; Zabihiyeganeh, M.; Rahimi Foroushani, A.; Jazayeri, S. The effect of quercetin on inflammatory factors and clinical symptoms in women with rheumatoid arthritis: A double-blind, randomized controlled trial. J. Am. Coll. Nutr., 2017, 36(1), 9-15.
[http://dx.doi.org/10.1080/07315724.2016.1140093] [PMID: 27710596]
[87]
Smolińska, E.; Węgrzyn, G.; Gabig-Cimińska, M. Genistein modulates gene activity in psoriatic patients. Acta Biochim. Pol., 2019, 66(1), 101-110.
[http://dx.doi.org/10.18388/abp.2018_2772] [PMID: 30904922]
[88]
Valensi, P.E.; Behar, A.; de Champvallins, M.M.; Attalah, M.; Boulakia, F.C.; Attali, J.R. Effects of a purified micronized flavonoid fraction on capillary filtration in diabetic patients. Diabet. Med., 1996, 13(10), 882-888.
[http://dx.doi.org/10.1002/(SICI)1096-9136(199610)13:10<882::AID-DIA247>3.0.CO;2-4] [PMID: 8911782]
[89]
Zhang, K.; Wang, Y.; Ma, W.; Hu, Z.; Zhao, P. Genistein improves thyroid function in Hashimoto’s thyroiditis patients through regulating Th1 cytokines. Immunobiology, 2017, 222(2), 183-187.
[http://dx.doi.org/10.1016/j.imbio.2016.10.004] [PMID: 27729167]
[90]
Niedelman, M.L.; Horoschak, S. Hesperidin and hesperidin with ascorbic acid in treatment of psoriasis. Arch. Dermatol., 1948, 57(2), 271-273.
[http://dx.doi.org/10.1001/archderm.1948.01520140133018] [PMID: 18912489]
[91]
Firestein, G.S. Evolving concepts of rheumatoid arthritis. Nature, 2003, 423(6937), 356-361.
[http://dx.doi.org/10.1038/nature01661] [PMID: 12748655]
[92]
Hsieh, P.H.; Wu, O.; Geue, C.; McIntosh, E.; McInnes, I.B.; Siebert, S. Economic burden of rheumatoid arthritis: A systematic review of literature in biologic era. Ann. Rheum. Dis., 2020, 79(6), 771-777.
[http://dx.doi.org/10.1136/annrheumdis-2019-216243] [PMID: 32245893]
[93]
Kvien, T.K.; Uhlig, T.; Ødegård, S.; Heiberg, M.S. Epidemiological aspects of rheumatoid arthritis: The sex ratio. Ann. N.Y. Acad. Sci., 2006, 1069(1), 212-222.
[http://dx.doi.org/10.1196/annals.1351.019] [PMID: 16855148]
[94]
van der Woude, D.; van der Helm-van Mil, A.H.M. Update on the epidemiology, risk factors, and disease outcomes of rheumatoid arthritis. Best Pract. Res. Clin. Rheumatol., 2018, 32(2), 174-187.
[http://dx.doi.org/10.1016/j.berh.2018.10.005] [PMID: 30527425]
[95]
Rudan, I.; Sidhu, S.; Papana, A.; Meng, S.J.; Xin-Wei, Y.; Wang, W.; Campbell-Page, R.M.; Demaio, A.R.; Nair, H.; Sridhar, D.; Theodoratou, E.; Dowman, B.; Adeloye, D.; Majeed, A.; Car, J.; Campbell, H.; Wang, W.; Chan, K.Y. Prevalence of rheumatoid arthritis in low- and middle-income countries: A systematic review and analysis. J. Glob. Health, 2015, 5(1), 010409.
[PMID: 25969732]
[96]
Ni, X.; Lai, Y. Keratinocyte: A trigger or an executor of psoriasis? J. Leukoc. Biol., 2020, 108(2), 485-491.
[http://dx.doi.org/10.1002/JLB.5MR0120-439R] [PMID: 32170886]
[97]
Michalek, I.M.; Loring, B.; John, S.M. A systematic review of worldwide epidemiology of psoriasis. J. Eur. Acad. Dermatol. Venereol., 2017, 31(2), 205-212.
[http://dx.doi.org/10.1111/jdv.13854] [PMID: 27573025]
[98]
Rachakonda, T.D.; Schupp, C.W.; Armstrong, A.W. Psoriasis prevalence among adults in the United States. J. Am. Acad. Dermatol., 2014, 70(3), 512-516.
[http://dx.doi.org/10.1016/j.jaad.2013.11.013] [PMID: 24388724]
[99]
Huang, T.H.; Lin, C.F.; Alalaiwe, A.; Yang, S.C.; Fang, J.Y. Apoptotic or antiproliferative activity of natural products against keratinocytes for the treatment of psoriasis. Int. J. Mol. Sci., 2019, 20(10), 2558.
[http://dx.doi.org/10.3390/ijms20102558] [PMID: 31137673]
[100]
Bonesi, M.; Rosa Loizzo, M.; Provenzano, E.; Menichini, F.; Tundis, R. Anti-psoriasis agents from natural plant sources. Curr. Med. Chem., 2016, 23(12), 1250-1267.
[http://dx.doi.org/10.2174/0929867323666160321121819] [PMID: 26997153]
[101]
Koblovská, R.; Macková, Z.; Vítková, M.; Kokoška, L.; Klejdus, B.; Lapčík, O. Isoflavones in the rutaceae family: Twenty selected representatives of the generacitrus, fortunella, poncirus, ruta andseverinia. Phytochem. Anal., 2008, 19(1), 64-70.
[http://dx.doi.org/10.1002/pca.1016] [PMID: 17654537]
[102]
Katsarou, A.; Gudbjörnsdottir, S.; Rawshani, A.; Dabelea, D.; Bonifacio, E.; Anderson, B.J.; Jacobsen, L.M.; Schatz, D.A.; Lernmark, Å. Type 1 diabetes mellitus. Nat. Rev. Dis. Primers, 2017, 3(1), 17016.
[http://dx.doi.org/10.1038/nrdp.2017.16] [PMID: 28358037]
[103]
Van Belle, T.L.; Coppieters, K.T.; Von Herrath, M.G. Type 1 diabetes: Etiology, immunology, and therapeutic strategies. Physiol. Rev., 2011, 91(1), 79-118.
[http://dx.doi.org/10.1152/physrev.00003.2010] [PMID: 21248163]
[104]
Maahs, D.M.; West, N.A.; Lawrence, J.M.; Mayer-Davis, E.J. Epidemiology of type 1 diabetes. Endocrinol. Metab. Clin. North Am., 2010, 39(3), 481-497.
[http://dx.doi.org/10.1016/j.ecl.2010.05.011] [PMID: 20723815]
[105]
Association, A.D. Diagnosis and classification of diabetes mellitus. Diabetes Care, 2009, 32(Suppl. 1), S62-S67.
[http://dx.doi.org/10.2337/dc09-S062] [PMID: 19118289]
[106]
Parvathaneni, A.; Fischman, D.; Cheriyath, P. Hashimoto’s thyroiditis. a new look at hypothyroidism. Intechopen, 2012, 2012, 4.
[107]
Zaletel, K.; Gaberšček, S. Hashimotos thyroiditis: From genes to the disease. Curr. Genomics, 2011, 12(8), 576-588.
[http://dx.doi.org/10.2174/138920211798120763] [PMID: 22654557]
[108]
Whitacre, C.C. Sex differences in autoimmune disease. Nat. Immunol., 2001, 2(9), 777-780.
[http://dx.doi.org/10.1038/ni0901-777] [PMID: 11526384]
[109]
Pearce, E.N.; Farwell, A.P.; Braverman, L.E. Thyroiditis. N. Engl. J. Med., 2003, 348(26), 2646-2655.
[http://dx.doi.org/10.1056/NEJMra021194] [PMID: 12826640]
[110]
Liverani, E.; Scaioli, E.; Digby, R.J.; Bellanova, M.; Belluzzi, A. How to predict clinical relapse in inflammatory bowel disease patients. World J. Gastroenterol., 2016, 22(3), 1017-1033.
[http://dx.doi.org/10.3748/wjg.v22.i3.1017] [PMID: 26811644]
[111]
Ungaro, R.; Mehandru, S.; Allen, P.B.; Peyrin-Biroulet, L.; Colombel, J.F. Ulcerative colitis. Lancet, 2017, 389(10080), 1756-1770.
[http://dx.doi.org/10.1016/S0140-6736(16)32126-2] [PMID: 27914657]
[112]
Hendrickson, B.A.; Gokhale, R.; Cho, J.H. Clinical aspects and pathophysiology of inflammatory bowel disease. Clin. Microbiol. Rev., 2002, 15(1), 79-94.
[http://dx.doi.org/10.1128/CMR.15.1.79-94.2002] [PMID: 11781268]
[113]
Teruel, C.; Garrido, E.; Mesonero, F. Diagnosis and management of functional symptoms in inflammatory bowel disease in remission. World J. Gastrointest. Pharmacol. Ther., 2016, 7(1), 78-90.
[http://dx.doi.org/10.4292/wjgpt.v7.i1.78] [PMID: 26855814]
[114]
Haskey, N.; Gibson, D. An examination of diet for the maintenance of remission in inflammatory bowel disease. Nutrients, 2017, 9(3), 259.
[http://dx.doi.org/10.3390/nu9030259] [PMID: 28287412]
[115]
Lee, D.; Albenberg, L.; Compher, C.; Baldassano, R.; Piccoli, D.; Lewis, J.D.; Wu, G.D. Diet in the pathogenesis and treatment of inflammatory bowel diseases. Gastroenterology, 2015, 148(6), 1087-1106.
[http://dx.doi.org/10.1053/j.gastro.2015.01.007] [PMID: 25597840]
[116]
Cirmi, S.; Navarra, M.; Woodside, J.V.; Cantwell, M.M. Citrus fruits intake and oral cancer risk: A systematic review and meta-analysis. Pharmacol. Res., 2018, 133, 187-194.
[http://dx.doi.org/10.1016/j.phrs.2018.05.008] [PMID: 29753688]
[117]
Marino, A.; Paterniti, I.; Cordaro, M.; Morabito, R.; Campolo, M.; Navarra, M.; Esposito, E.; Cuzzocrea, S. Role of natural antioxidants and potential use of bergamot in treating rheumatoid arthritis. PharmaNutrition, 2015, 3(2), 53-59.
[http://dx.doi.org/10.1016/j.phanu.2015.03.002]

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